Recreation Effects On Wildlife Research

RESEARCH ARTICLE
Effects of Recreation on Animals Revealed as

Widespread through a Global Systematic
Review
Courtney L. Larson1*, Sarah E. Reed1,2, Adina M. Merenlender3, Kevin R. Crooks1
1 Department of Fish, Wildlife, and Conservation Biology, Colorado State University, Fort Collins, Colorado,
United States of America, 2 North America Program, Wildlife Conservation Society, Bozeman, Montana,
United States of America, 3 Department of Environmental Science, Policy, and Management, University of
California-Berkeley, Berkeley, California, United States of America
* courtney.larson@colostate.edu
a11111
Abstract
OPEN ACCESS
Citation: Larson CL, Reed SE, Merenlender AM,
Crooks KR (2016) Effects of Recreation on Animals
Revealed as Widespread through a Global
Systematic Review. PLoS ONE 11(12): e0167259.
doi:10.1371/journal.pone.0167259
Editor: Hideyuki Doi, University of Hyogo, JAPAN
Received: December 1, 2015
Accepted: November 11, 2016
Published: December 8, 2016
Copyright: 2016 Larson et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: This study was funded by the California
Department of Fish and Game (Local Assistance
Grant P1182112). The funders had no role in study
design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Outdoor recreation is typically assumed to be compatible with biodiversity conservation and

is permitted in most protected areas worldwide. However, increasing numbers of studies are
discovering negative effects of recreation on animals. We conducted a systematic review of
the scientific literature and analyzed 274 articles on the effects of non-consumptive recreation on animals, across all geographic areas, taxonomic groups, and recreation activities.
We quantified trends in publication rates and outlets, identified knowledge gaps, and
assessed evidence for effects of recreation. Although publication rates are low and knowledge gaps remain, the evidence was clear with over 93% of reviewed articles documenting
at least one effect of recreation on animals, the majority of which (59%) were classified as
negative effects. Most articles focused on mammals (42% of articles) or birds (37%), locations in North America (37.7%) or Europe (26.6%), and individual-level responses (49%).
Meanwhile, studies of amphibians, reptiles, and fish, locations in South America, Asia, and
Africa, and responses at the population and community levels are lacking. Although
responses are likely to be species-specific in many cases, some taxonomic groups (e.g.,
raptors, shorebirds, ungulates, and corals) had greater evidence for an effect of recreation.
Counter to public perception, non-motorized activities had more evidence for a negative
effect of recreation than motorized activities, with effects observed 1.2 times more frequently. Snow-based activities had more evidence for an effect than other types of recreation, with effects observed 1.3 times more frequently. Protecting biodiversity from potentially
harmful effects of recreation is a primary concern for conservation planners and land managers who face increases in park visitation rates; accordingly, there is demand for sciencebased information to help solve these dilemmas.
Competing Interests: Adina Merenlender is on the

editorial board of PLOS ONE. This does not alter
the authors adherence to PLOS ONE editorial
policies and criteria.
PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016
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Systematic Review of Recreation Effects on Animals
Introduction
Visitation to protected areas, ranging in scope from international ecotourism to local park visits, was recently estimated at 8 billion visits per year [1]. In the United States, the number of
participants in outdoor recreation increased by 7.5% and total visitor days increased by 32.5%
between 2000 and 2009 [2]. Driven in part by rapid growth in international tourism [3], recreation and ecotourism are also expanding in the developing world [4]; visits to protected areas
in Africa, Asia, and Latin America increased by 2.5 to 5% between 1992 and 2006 [5].
Recreation is commonly assumed to be compatible with biodiversity conservation, in contrast to more well-known threats such as population growth and development at protected
area edges [6,7] or subsistence use within reserves to help sustain local livelihoods [8]. Most
protected areas have a dual mandate to conserve biodiversity and improve human welfare
through resource use or outdoor recreation [8,9]. Accordingly, recreation is permitted in over
94% of International Union for Conservation of Nature (IUCN) protected areas globally (categories Ib-VI; [10,11]). In the United States and other developed nations, providing opportunities for outdoor recreation has historically been an important reason for the designation of
protected areas [12], whereas in the developing world, ecotourism has been embraced as a
potential win-win solution for poverty alleviation and conservation [8]. Furthermore, there
are numerous benefits of outdoor recreation for human health and communities. People with
access to natural areas have lower mortality rates [13], and outdoor play promotes mental and
physical health in children [14]. Recreation and ecotourism can also be a source of economic
revenue for protected areas and the communities around them [15,16], and can help garner
support for conservation [17].
Despite these benefits, there is growing recognition that outdoor recreation can have negative impacts on biological communities. Recreation is a leading factor in endangerment of
plant and animal species on United States federal lands [18], and is listed as a threat to 188 atrisk bird species globally [19]. Effects of recreation on animals include behavioral responses
such as increased flight and vigilance [20,21]; changes in spatial or temporal habitat use
[22,23]; declines in abundance, occupancy, or density [9,24,25]; physiological stress [26,27];
reduced reproductive success [28,29]; and altered species richness and community composition [30,31]. Many species respond similarly to human disturbance and predation risk, meaning that disturbance caused by recreation can force a trade-off between risk avoidance and
fitness-enhancing activities such as foraging or caring for young [32].
Although there is a growing body of empirical studies of the effects of recreation on animals, a recent global review of the scientific literature does not exist. Early reviews [3336] provide valuable definitions and conceptual frameworks, but were not systematic and need
updating to reflect studies published in recent decades. In addition, contemporary reviews
have restricted their scope by location or habitat type [3739], taxonomic group [4045], or
recreation activity [4648].
We conducted a global review of the published scientific literature to synthesize effects of
non-consumptive recreation across all animal taxa. Such a review adds to the evidence base
necessary to help bridge the gap between conservation science and practice [49]. To aid decision-makers faced with dilemmas about managing the demand for recreation while trying to
fulfill mandates to protect species, it is critical to understand the degree to which biodiversity
conservation and recreation are compatible, and under what circumstances. First, we examined trends in recreation research, including publication rates over time, geographic distribution, and study design. Second, we investigated which taxonomic groups were most
commonly studied, and which had more or less evidence for effects of recreation. Similarly, we
investigated which recreation activities and types of responses (e.g., behavioral, abundance, or
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survival) were most frequently measured, and what effects were observed. Finally, we examined management strategies proposed by the authors to avoid or mitigate these effects.
Methods
Search strategy
Because our objective was to locate studies of all animal species and all types of recreation, our
search protocol was designed to produce a broad list of articles. We did not include taxonomic
keywords since titles and abstracts often refer only to the studys focal species. Instead, we limited the search to journals within four categories within the Institute for Scientific Information
Web of Science database (Thompson Reuters, New York, NY, USA) that were the most relevant to our goals: biodiversity conservation, ecology, zoology, and behavioral sciences. From
this list, we removed journals that were not published in English, or could not be reasonably
expected to publish articles on recreation and animals (n = 166 journals included in the final
list). We then searched the database with the Boolean search string: (ts = (touris OR recreat )
AND so = (journal list)), where ts indicates topic keywords and so restricts the search to the list
of 166 journals described above. This search strategy has high sensitivity (the proportion of all
relevant information that the search locates) and low specificity (the proportion of search
results that are relevant), which helps reduce bias and increase repeatability [50]. To reduce
the effect of dissemination bias in our analysis, we included articles published in regional and
lesser-known journals as well as the most widely-read publications [51]. Since our search strategy made use of the journal category feature within Web of Science, we were not able to replicate the search in other databases. However, our strategy produced a more thorough and
comprehensive list of articles than if we had restricted our search with taxonomic keywords.
Screening and data extraction

Our keyword search (performed 30 January 2013 and again on 21 March 2016) resulted in a
comprehensive list of 2,306 articles. We first reviewed titles and abstracts and eliminated obviously irrelevant records (e.g., tourism management papers with no wildlife component; Fig 1).
We then reviewed the full text of the remaining 403 articles and assessed them against our
inclusion criteria, recording the reason for rejection if necessary [50]. We excluded consumptive activities, which we define following Duffus and Dearden [34] as activities that purposefully remove or permanently affect wildlife (e.g., hunting, fishing). We focused on nonconsumptive forms of recreation (e.g., hiking, skiing) because these activities are permitted
more widely throughout protected areas. However, studies examining consumptive activities
as a source of disturbance for non-target species (e.g., effects of fishing on waterbirds; [52])
were retained. We also rejected articles if they did not study one or more animal species (n =
2), did not test effects of non-consumptive recreation via a statistical test (n = 70), did not collect empirical field data (e.g., were review or simulation articles; n = 23), studied the effects of
recreation infrastructure independently of human activity (e.g., presence of ski lifts; n = 20), or
examined recreation as a vector for invasive species dispersal (n = 14). Experimental treatments designed to mimic recreational activities were included. The final list included 274 articles (S1 Appendix) with 2,048 distinct results.
Data collected from each article included publication information, geographic location
(country and continent), study design, taxonomic group(s), recreation activities, response
types and effects found, and management recommendations (Table 1). For articles that studied
multiple species, recreation activities, or response types, we treated each combination of variables as a separate result, rather than attempting to determine an overall effect for each article, which would ignore valuable findings from within each article. For example, Banks and
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Fig 1. PRISMA literature search flow diagram. The number of studies that were located, retained, and discarded are shown
at each stage of the literature review process.
doi:10.1371/journal.pone.0167259.g001
Bryant [24] examined the effects of hiking and dog-walking on bird abundance and richness,
so we recorded four combinations of results in our database. While results from the same
study often rely on the same animal populations, locations, and data collection efforts, we
examined each result separately since effects often differed. Because each article could be considered an experimental unit, we added a random effect for article in the analysis to control for
this potentially confounding factor (see Statistical analysis).
The effect variable (Table 1), which was the response variable for several of our research
questions, was a binary variable indicating whether the recreation effect documented by the
authors was statistically significant (as defined by the authors). We categorized all significant
effects as negative, positive, or unclear. Negative responses were consistent with the following
effects of recreational disturbance at the community, population, or individual (behavioral or
physiological) levels: decreased species richness or diversity; decreased survival, reproduction,
occurrence, or abundance; behaviors typically assumed to reflect negative responses to anthropogenic disturbance (e.g., decreased foraging or increased vigilance); and physiological condition typically assumed to reflect disturbance effects (e.g., decreased weight or increased stress).
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Table 1. List of variables collected from articles included in the review of the effects of non-consumptive recreation on animals.
Category
Variable
Publication
Author(s)
Description or list of categories
text
Title
text
Journal
Journal type
Geographic
categorical
numeric
Continent
categorical
Country
text
Study design Measure of

recreation*
Taxonomic
text
Behavior, conservation, ecology, ecosystem/region-specific, general biology, taxa-specific, zoology/
wildlife, other
Publication year
Habitat type
Effect
Data type
Agricultural, beach, desert, forest, freshwater, grassland, marine, polar, shoreline, urban, scrub/shrub,
tundra, wetland, other
categorical
Direct observation, experimental treatment, expert opinion, remote monitoring, permitted use, proxy
categorical
Experiment
Was it an experimental study?
yes/no
Control
Did the study include a control treatment? (e.g. a no-recreation site)
yes/no
Replication
Did the study replicate treatments, study sites, observation periods, etc?
yes/no
Effect*
Did the authors find a significant recreation impact?
yes/no
Effect direction*
Positive, negative, unclear
categorical
Multiple species
Were multiple species studied?
yes/no
Taxa group
Amphibian, bird, fish, invertebrate, mammal, reptile
categorical
Scientific name*
text
Common name*
text
Recreation
Activity*
Alpine skiing, beach use, biking, boating (non-motorized), camping, nordic ski/snowshoeing, dogwalking, equestrian, hiking/running, motorized (boat), motorized (land), motorized (snow), swimming/
diving, wildlife feeding, wildlife viewing (boat), wildlife viewing (land), other (aquatic), other (terrestrial)
categorical
Response
Type*
Abundance, behavioral, community (species richness, diversity, or composition), occurrence,

physiological, reproductive, survival, other
categorical
Cap visitation, improve infrastructure, rule change, staff training, spatial restrictions, temporal
restrictions, visitor education, none, other
categorical
Management Recommendations
* For articles that studied multiple species, recreation activities, or response variables, we treated each combination of variables as a separate result, and
recorded the information marked with an asterisk (*) for each result individually.
doi:10.1371/journal.pone.0167259.t001
Conversely, positive responses were in the opposite direction. We were unable to classify some
responses as positive or negative and labeled them unclear. Examples of unclear effects were
behavioral responses that did not have obvious fitness consequences (e.g., decreased vocalizing) and results with non-linear responses (e.g., highest reproductive success at an intermediate level of recreation). We note that positive responses do not necessarily imply beneficial
outcomes for biodiversity conservation; for example, an increase in species richness could be
attributable to an increase in non-native species.
We caution that a statistically significant effect of recreation does not necessarily provide
insight into the effects magnitude or biological significance. Authors may also include statistically significant results while omitting non-significant findings due to publication bias [53]. A
formal meta-analysis framework can help researchers summarize effect sizes and detect and
adjust for publication bias [54], but the study design must be similar across all studies
included, with comparable predictor and response variables [55]. This was not feasible given
the broad scope of our review, and accordingly, we do not make statistical comparisons
among groups. Ultimately, we believe our approach provides a meaningful representation of
the weight of evidence that currently exists.
5 / 21
Publication trends and geographic distribution

We summarized the number of articles by publication year, journal type, country, continent,
and habitat type. Journals were classified into eight broad types using the journal title and
online aims and scope statement to identify the appropriate primary category. Articles were
also assigned to one or more habitat classes on the basis of authors descriptions (Table 1).
Study design
To examine how recreation studies have been designed and conducted, we recorded the proportion of articles that used an experimental design and included controls and replication. For
our purposes, any kind of an experimental treatment (e.g., experimental boat passes near a raptor nest; [56]) counted as an experimental design, and any treatment or site without recreation
counted as a control. We also examined the method used to measure recreation: direct observation (with human observers), experimental treatment (e.g., researchers simulating recreation
activities), expert opinion, remote monitoring (e.g., automatic counters), permitted use (e.g.,
whether a site was open to a specific recreational activity), or proxy variables (e.g., car counts).
Taxonomic groups
We examined differences in research focus and evidence for recreation effects among six
broad taxonomic groups: amphibians, birds, fish, invertebrates, mammals, and reptiles. We
divided groups with sufficient sample size ( 15 results on 3 different species) into narrower
taxonomic classifications (Classes for invertebrates and fish; Orders for birds, mammals, and
reptiles; amphibians were omitted due to small sample size). We then subdivided Classes or
Orders with sufficient sample sizes ( 15 results on 3 different species) once again into
Orders or Families. We also grouped species by their IUCN status [57].
Recreation activities
We grouped recreation activities into 18 types (Table 1) and created broader categories for
more general comparisons: winter terrestrial (snow and ice-based activities such as skiing and
snowmobiling), summer terrestrial (land activities not requiring snow or ice), and aquatic
activities. We also compared motorized and non-motorized activities.
Response types
We categorized animal responses into eight types: community (species richness, diversity, or
composition metrics), survival, reproduction, abundance, occurrence, behavior, and physiological measures, as well as other responses (e.g., sex ratio). For more general comparisons,
we also grouped the response types hierarchically into community-, population- (survival,
reproduction, abundance, and occurrence), and individual-level (behavior and physiological)
responses.
Management recommendations
To qualify the management recommendations noted in the articles and provide a useful synthesis for land managers, we categorized recommended management actions as follows: spatial
restrictions, capping visitation, increasing visitor education, temporal restrictions, improving
infrastructure, adding or changing rules, enforcement of existing rules, staff training, or
other (Table 2). Calls for additional research, although common in the literature, were not
considered to be management recommendations.
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Table 2. General management recommendations suggested by authors of articles included in the review.
Recommendation
Examples
Frequency
(%)*
Spatial restrictions
Designate a trail-free area within protected area; establish minimum approach distances to animals
32.1
Visitor education
Educate SCUBA divers about the impacts of human contact on coral; instruct visitors about effects of noise on
sensitive species
15.0
Cap visitation
Limit the number of visitors that can enter the area per day
14.2
Temporal restrictions
Limit recreational access during the breeding season
13.1
Rule change
Restrict boat speed in sensitive areas; prohibit wildlife feeding
9.9
Physical
improvements
Restore habitat; install fencing around sensitive areas
9.5
Other
Species translocations; increased use of private land for conservation
8.8
Enforcement
Enforce leash laws; keep people on trails
6.9
Staff training
Train staff to recognize signs of animal disturbance
2.2
No recommendations
40.5
* Percentages do not sum to 100 because some articles made more than one management recommendation.
doi:10.1371/journal.pone.0167259.t002
Statistical analysis
We used linear regression to assess trends in the total number of articles over time as well as
the proportion of included articles out of the total publication volume in the selected journals.
To assess gaps in the literature, we used chi-square goodness of fit tests to determine if the distribution of articles differed significantly from an expected distribution. For journal type, the
expected distribution was the proportion of journals in the journal set that belonged to each
type. For geographic distribution, we compared the distribution of articles by continent to the
total land area and human population density of each continent. For IUCN status and taxonomic groups, the expected distribution was the number of known species in each group,
starting with the broadest groups and progressing down to Family when possible [57]. We did
not use chi-square tests if articles were counted under more than one category (e.g., articles
examining multiple types of recreation, such as hiking, biking, and equestrian) since this violates the assumption of independence.
We estimated the amount of evidence for a recreation impact as the overall percentage of
results that found a statistically significant effect of recreation. These percentages were estimated for results summarized by taxonomic groups, recreation activities, and response types.
Because most articles included multiple results, the percentages ( SE) we report are leastsquares means and standard errors obtained from models that included article as a random
effect. We used generalized linear mixed models (GLMMs) with a logit link function to estimate the frequency of overall effects among taxonomic groups, recreation activities, and
response types, and we used proportional odds models [58] to estimate the proportion of overall effects that were negative, positive, or unclear. All statistical analyses were conducted in R
using packages lme4, ordinal, and lsmeans [5962].
Results
Publication trends and geographic distribution
The earliest articles discovered by our search were published in 1981, and the peak year was
2008 with 23 articles. The number of articles published per year that met our criteria increased
23.5% on average per year from 1981 to 2015 ( = 0.66, 95% CI = (0.53, 0.80), p < 0.0001).
This increase was not solely a result of increasing publication volume; the proportion of
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Fig 2. Published articles on the effects of non-consumptive recreation on animals by publication

year. The numbers of articles are shown as raw numbers (shaded bars) and as percentages of the overall
publication volume in the journal set used in this review (trendline; a second order polynomial function).
included articles out of the total articles published in the journal set increased by 8.8% on average per year ( = 0.000043, 95% CI = (0.000033, 0.000053), p < 0.0001; Fig 2). The distributions of the journal set into journal types (e.g., conservation, wildlife) and individual articles
into journal types were significantly different (2 = 632.4, df = 7, p < 0.0001). Most of the
included articles were published in conservation (38.7%) and wildlife (19.7%) journals, followed by ecology (13.5%), taxa-specific (13.1%), ecosystem or region-specific (9.9%), and
behavior journals (3.3%); very few articles were published in general biology (0.7%) or other
(0.7%) journal categories.
Geographically, studies of recreation on animals were conducted mostly in North America
(37.7%), Europe (26.6%), and Oceania (13.1%), and relatively few in South America (9.1%),
Asia (5.5%), Africa (5.1%), and Antarctica (2.9%; Fig 3A). This distribution among continents
was not proportional to the land area (2 = 366.3, df = 6, p < 0.0001) nor human population
density (2 > 500, df = 6, p < 0.0001) of the continents. The United States accounted for 27.0%
of the articles, followed by Australia (7.7%), Spain (5.8%), New Zealand (5.5%), the United
Kingdom (4.7%), Argentina (4.4%), and Canada (4.4%). Most studies were conducted in forest
(35.4%), marine (23.4%), grassland (15.7%), and shoreline (13.9%) habitats (Fig 3B). The least
well-studied habitat types were polar (2.9%), and desert (1.5%), as well as human-modified
habitats (agricultural and urban, representing 10.2% of articles combined).
Study design
Less than one-third (30.3%) of the articles contained an experimental component, and 60.9%
of articles contained controls. Most (85.4%) articles had replication of study sites, treatments,
or groups. Direct observation was the most common method for measuring recreation (38.1%
of results), followed by proxy variables (19.9%), expert opinion (19.6%), and experimental
treatment (18.0%). Permitted use as a measure of recreation was less common (12.5%), as was
remote monitoring (6.7%).
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Fig 3. Distribution of published articles on the effects of non-consumptive recreation on animal species. Panel (a)
shows the countries where studies were conducted, and panel b) shows the distribution of studies into major habitat type
(s). Since some studies involved multiple habitat types, the sum (424) is greater than the total number of articles (274).
Numbers at the end of bars represent the total number of articles in each category.
Taxonomic groups
Research effort in our sample of articles was not proportional to the number of species within
all taxonomic groups at the broadest level (2 = 377.3, df = 5, p < 0.0001), nor to the number
of species in bird (2 = 988.7, df = 5, p < 0.0001) and mammal (2 = 290.3, df = 3, p < 0.0001)
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Orders or invertebrate Classes (2 = 98.1, df = 2, p < 0.0001; Fig 4). Mammals (41.6%) and
birds (36.9% of articles) were the focus of the majority of recreation studies, followed by invertebrates (12.4%), reptiles (5.5%), fish (5.1%), and amphibians (0.7%). Studies of a single species
were more common (69.0%) than those that examined at least two species. Research on mammals focused mainly on ungulates (28.9%), carnivores (26.3% of articles), cetaceans (21.9%),
and primates (12.3%). Among birds, the most commonly researched Orders were Passeriformes (passerine birds; 24.8% of articles), Charadriiformes (wading birds and gulls; 23.8%),
Sphenisciformes (penguins; 13.9%), and Accipitriformes (hawks, eagles, vultures; 9.9%). Many
of the invertebrate studies (35.2%) focused on the effects of snorkeling or SCUBA diving on
corals, followed by studies on arachnids, bivalves, and insects (each 14.7%). The most commonly studied fish Class was Actinopterygii (ray-finned fish; 57.1%), followed by Chondrichthyes (sharks, stingrays; 42.9%). Research on reptiles focused on Orders Squamata
(lizards, snakes; 78.6%) and Testudines (turtles; 21.4%).
We identified the IUCN status of the species for 68.7% of results, representing 305 unique
species; the remaining results examined multiple species or species not evaluated by the IUCN.
The distribution of these results into IUCN status categories was not proportional to the distribution of all animal species into these categories (2 = 108.3, df = 5, p < 0.0001), with many
more species than expected in the least concern category (80.7%), slightly more than expected
in the near threatened (6.9%), and fewer than expected in the data deficient (1.6%), vulnerable
(6.5%), endangered (3.6%), and critically endangered (0.1%) categories. Endangered species
that were studied included three mammals (black howler monkey Alouatta pigra, Hectors dolphin Cephalorhynchus hectori, and the Barbary macaque Macaca sylvanus), three fish (dusky
grouper Epinephelus marginatus, Nassau grouper Epinephelus striatus, and the brownstriped
gaunt Anisotremus moricandi), two birds (Egyptian vulture Neophron percnopterus and the yellow-eyed penguin Megatypes antipodes), two reptiles (wood turtle Glyptemys insculpta and Lilfords wall lizard Podarcis lilfordi), and the boulder star coral Montastraea annularis. The only
critically endangered animals were the Western lowland gorilla Gorilla gorilla gorilla and the
Mexican howler monkey Alouatta palliata mexicana.
Of the 274 articles analyzed, 93.1% documented at least one effect of recreation on animal
populations, individuals, or communities. Negative effects of recreation were the most frequent (59.4%), followed by unclear (25.9%) and positive (14.7%) effects. Most (83.6%) of the
unclear effects were behavioral responses.
Taxonomic groups with the most negative effects were amphibians (68.4 20.2% of
results), reptiles (56.3 9.2%), and invertebrates (51.0 5.1%), while mammals (5.3 1.9%)
and birds (4.3 2.0%) had the most positive effects (Fig 4). Among bird Orders, evidence for
overall and negative effects was greatest in Accipitriformes (e.g., eagles, hawks; 70.7 10.7 and
47.7 24.4%; Fig 4). Positive effects were greatest in Anseriformes (e.g., ducks, swans;
10.4 22.6%) and Passeriformes (passerine birds; 6.9 7.7%). Evidence of negative effects
among Charadriiformes Families was greatest in Charadriidae (e.g., plovers, lapwings;
58.2 18.6%). Among Passeriformes Families, Corvidae (e.g., crows, choughs) had the most
positive effects (56.0 4.9%). Among mammal Orders, Artiodactyla (even-toed ungulates)
had the most negative effects (48.5 8.0%) and Rodentia (rodents) had the most positive
effects (14.4 12.3%). At the family level, Bovidae (e.g., bison, bighorn sheep) had by far the
most overall effects (93.8 19.3%) and Delphinidae (dolphins) was also high (70.8 6.8%).
Several invertebrate Classes had considerable negative effects, including Anthozoa (corals;
56.6 4.2%), Gastropoda (e.g., snails, slugs; 55.5 6.7%), and other (e.g., insects, crabs;
51.4% 6.0%). Finally, the other grouping of fish Classes (e.g., sharks, stingrays) had more
evidence for an overall and positive effect (64.9 8.7% overall and 25.8 15.7% positive) than
Actinopterygii (ray-finned fish; 34.8 8.5% overall and 5.4 9.2% positive). Of the reptile
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Fig 4. Evidence for an effect of recreation by taxonomic group. Evidence is measured as the proportion of results that were
statistically significant. For articles that studied multiple recreation activities, species, or response variables, each combination of
variables was treated as a separate result. Common names are examples of species occurring in the included articles. We
present taxonomic groups that have at least 15 results and 5 species represented; the remaining taxa are included in other
categories for comparative purposes. Numbers following bars show the number of results, number of articles, and count of
unique species. Articles that studied functional groups or communities rather than individual species (e.g., insectivorous birds)
were added to the relevant other category and were not counted as species. Error bars show standard error for the sum of all
effects.
orders, Order Testudines (turtles) had more overall effects (75.0 12.5%) effects than Order
Squamata (lizards, iguanas; 52.3 7.5). For both Orders, all of the effects were negative. Low
sample sizes precluded comparisons among amphibian taxa.
Recreation activities
The articles in our sample examined a wide variety of recreation activities (Fig 5A). Summer
terrestrial activities were the most common, studied by 66.7% of articles, followed by aquatic
(27.8%) and winter terrestrial (5.6%). Motorized forms of recreation, including off-highway
vehicles, snowmobiles, and motorized boats, were examined in 26.3% of articles. Hiking was
studied much more often than any other recreation activity (27.5% of articles). Wildlife viewing was also relatively frequently studied, with 10.3% of articles studying land-based and 6.6%
studying boat-based wildlife viewing.
Winter terrestrial activities had the most evidence of overall (77.3 7.8% of results; Fig 5B)
and negative (64.4 10.1%) effects, compared to 58.5 2.7% (overall) and 39.6 4.6% (negative) for other terrestrial and 57.0 3.8% (overall) and 33.4 7.1% (negative) for aquatic activities. Although motorized and non-motorized activities had similar evidence for overall effects
(57.0 5.1% and 58.4 2.5%), non-motorized had greater negative effects (40.3 4.0% versus
34.0 8.6%). Activities with the most evidence of overall effects included each of the snow
activities (cross-country ski/snowshoeing: 81.0 8.6%, motorizedsnow: 77.8 13.9%, alpine
skiing: 71.0 8.2%), as well as boat-based wildlife viewing (65.4 5.4%) and beach use
(64.8 8.2%; Fig 5B).
Response types
Response types were not studied evenly; behavioral (45.5% of articles) and abundance (24.1%)
responses to recreation were the most common (Fig 6A). Only 9.3% of articles measured community metrics (species richness, diversity, or composition) and 1.9% measured survival.
Omitting survival responses due to small sample size, community responses had the most
overall effects (64.6 6.6% of results), followed by behavioral (63.5 2.8%) and physiological
(62.5 4.9%) responses; reproductive responses (36.7 6.3%) had the fewest overall effects
(Fig 6B). Physiological (52.7 4.8%) and occurrence (51.3 4.6%) responses had the most
negative effects, while behavioral responses had the most positive effects (9.8 2.5%).
Management recommendations
More than one-third (40.5%) of the included articles did not provide management recommendations (Table 2). Of those that did include recommendations, the most common types were
spatial restrictions (32.1%), visitor education (15.0%), and limiting visitation (14.2%), Enforcement of existing rules (6.9%) and staff training (2.2%) were the least frequently suggested management categories.
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Fig 5. Recreation activities in the articles included in this review. Panel (a) shows the percent of articles that included each
recreation activity (numbers of articles follow the bars), and panel (b) shows the percent of results in which a statistically
significant effect of recreation on an animal species was observed (number of results follow the bars). Total percentages are
divided into negative, positive, and unclear effects of recreation. Error bars show standard error for the sum of all effects.
Discussion
Although published research on recreation effects on animals increased by an order of magnitude from 1981 to 2015, the percentage of the literature devoted to the subject remains small
(0.16% of publication volume of the target journals in the peak year), and many gaps in knowledge remain. The literature is geographically biased in favor of North America and Europe,
and taxonomically biased toward birds and mammals. Over 93% of reviewed articles documented at least one effect of recreation, and as expected, the majority of these effects were negative. Non-motorized and winter terrestrial activities had notable evidence for negative effects.
Additionally, some of the least studied taxonomic groups (reptiles, amphibians, and invertebrates) had the greatest evidence for negative effects of recreation.
Though the amount of literature on this topic has increased in recent decades, it may not be
reaching a broad audience even among conservation scientists and wildlife ecologists. Over
20% of articles were published in journals specific to a taxonomic group, geographic region, or
ecosystem, whereas few were published in the broadest journals. Since the broadest journals
are also among the highest-impact publications (e.g., Science, Nature), this could also indicate
that the topic of recreation impacts on animals is not viewed as important within the peerreviewed literature.
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Fig 6. Types of animal responses to recreation in the articles included in this review. Response types have been categorized
into community-, population-, and individual-level responses. Panel a) shows the percent of articles in which each response type is
tested (numbers of articles follow the bars). Panel b) shows the percent of results in which a statistically significant effect of recreation
on an animal species was observed (number of results follow the bars). Total percentages are divided into negative, positive, and
unclear effects of recreation. Error bars show standard error for the sum of all effects.
The articles had a strong geographic bias toward North America and Europe. This reflects
global patterns in visitation to protected areas since over 80% of visits occur in these two continents [1]. A surprising number of studies were conducted in Antarctica, as a result of a growing ecotourism industry that often includes visits to penguin colonies [63]. As South America,
Africa, and Asia contain most of the worlds biodiversity hotspots [64] as well as popular ecotourism destinations including Brazil, South Africa, Thailand, and Indonesia [65], we see an
immediate need for studies of recreation effects in these areas. The few studies conducted in
tundra, polar, and desert habitat types is likely a result of low rates of recreation and tourism
occurring in these areas. However, our findings and those of Sato et al. [39] about the impacts
of alpine activities indicate that it is an important area for future study.
Further, the distribution of articles among broad taxonomic groups was skewed in favor of
mammals and birds, a trend consistent with conservation science as a whole [66]. However,
these are large, diverse groups that still warrant more research; for example, passerine birds
were the most frequently studied avian Order in our set of articles, but the 73 species examined
therein comprise ~1% of the 5,000+ species in the Order. There is also an urgent need to
understand more about the potential effects of recreation on invertebrates, fish, reptiles, and
amphibians. We found only two articles on amphibians, but their known sensitivity to human
disturbance [67] highlights the need to understand whether and how recreation affects them.
Current research on recreation effects on animals does not include many species of urgent
conservation concern; only about 10% of species studied are globally threatened (IUCN status
of critically endangered, endangered, or vulnerable). Recreation may not be the primary reason for their endangerment, but it is a threat worth understanding because the disturbance
may take place in the very protected areas designated to conserve these species. Finally, relatively few articles (31.0%) examined more than one species, and studies of species from
14 / 21
multiple trophic levels were especially rare (3.6%). More research is needed on communitylevel effects of recreation, including potential cascading effects [68].
Examination of the study designs of the included articles revealed some notable trends. A
fairly high percentage (30%) of articles included an experimental component; most of these
were recreation treatments applied in order to compare behavioral responses. Over 80% of
results examined recreation as a categorical variable, typically with three or fewer levels (e.g.,
low vs. high recreation activity). Though a categorical approach is simpler to implement and
analyze, it limits the ability of researchers to evaluate how responses may change with different
recreation intensities. It has proven difficult to develop hypothesized response curves representing how animals respond to increasing levels of recreational use due to the diversity of
responses [69]. Future research should measure recreation across intensity gradients to help
verify the existence of thresholds and the shape of these relationships.
Most (59%) of the effects of recreation on animals documented in the reviewed articles
were negative effects. This was particularly true for reptiles, amphibians, and invertebrates,
although sample sizes were low. Among invertebrate Classes, Anthozoa (corals) frequently had
physical damage or reduced abundance in areas frequented by recreational divers [70,71].
Though the rate of negative effects was generally lower for birds, mammals, and fish, some
lower taxonomic groups had more evidence for negative effects of recreation. For example,
Order Accipitriformes (e.g., eagles, hawks) had more evidence for negative effects compared
to other bird Orders, consistent with a prior meta-analysis of human disturbance on nesting
birds of prey [41]. Family Charadriidae (e.g., plovers, lapwings) also had considerable evidence
for negative effects of recreation, which parallels a recent study that found that species from
this Order (Charadriiformes) were more frequently threatened by tourism than other bird
Orders [19]. Of the mammals, Order Artiodactyla (e.g., deer, bison) had substantial evidence
for negative effects, mostly consisting of behavioral responses to recreation activity. Many
researchers have investigated factors that influence ungulate flight responses, including speed
of approach, animal and human group size, and habitat type [43,45]. For fish, several studies
found negative physiological effects of wildlife viewing on Class Chondrichthyes (e.g., sharks,
stingrays; [72,73]), and negative effects of diving on fish communities [70].
Evidence for positive effects of recreational activity was much less common. Birds, particularly corvids, had more evidence for positive effects compared to most other broad taxonomic
groups. Many corvids are urban adaptors [74], and several studies found that they quickly
habituate to human disturbance, allowing them to tolerate or even thrive in the presence of
recreationists [75,76], sometimes at the expense of other species [77]. Mammals also had a relatively high rate of positive effects. Of the mammal Orders, rodents had the most evidence for
positive effects; all but one of these effects were behavioral and most resulted from habituation
(e.g., reduced flight responses in areas with higher levels of recreation; [78,79]. Habituation to
recreation was discussed in many (39.4%) of the included articles and typically resulted in positive responses in our coding system (e.g., reduced flight initiation distances in habituated animals), but whether habituation is a beneficial outcome for animals (e.g., by reducing costly
behavioral responses to humans) is unclear and warrants further study [80,81].
We found that non-motorized activities had more evidence for negative effects than motorized activities. Motorized activities are often expected to be more harmful to animals because
of vehicle speed and noise [43], but our results suggest the opposite across a wide range of
study locations and taxa. A few articles directly compared motorized and non-motorized activities; four mammals (guanaco Lama guanicoe, wolverine Gulo gulo, coyote Canis latrans, and
bobcat Lynx rufus) showed behavioral or occurrence responses to non-motorized but not to
motorized recreation [22,82,83], whereas the reverse was found for Hectors dolphin (Cephalorhynchus hectori) behavior [84] and ghost crab (Ocypode quadrata) abundance [85].
15 / 21
However, motorized activities often cover larger spatial extents than non-motorized activities,
and since most studies did not compare effects across multiple spatial scales, it is possible that
their impact has been underestimated. Additionally, motorized vehicles can also cause other
types of harm not explored here, such as soil loss and vegetation disturbance [86]. A metaanalysis designed to explicitly compare the magnitude of effects of motorized and non-motorized recreation would be a valuable contribution to the literature.
Our results also suggest that winter terrestrial activities have greater evidence for effects on
animals than summer terrestrial or aquatic activities, though the number of articles was small.
A recent review of winter recreation effects on animals [39] supports this conclusion, finding
that over half of the reviewed articles reported overall detrimental effects, particularly on birds
and on species richness and diversity. There are several possible explanations for this result.
Movement away from recreationists may be more energetically costly in snowy conditions
[87]. For many species, food availability and quality is lower during winter [82,88], limiting
their ability to relocate to avoid areas with human activity. There could also be habitat effects
since vegetation in alpine and sub-alpine environments regenerates slowly, so habitat degradation caused by winter recreation could be more severe than that caused by other recreational
activities in more temperate climates [39,89].
Overall, authors observed individual-level (behavioral and physiological) and communitylevel effects more frequently than most population-level (occurrence, abundance, and reproduction) effects. Though rarely measured, negative effects of recreation on survivala particularly important response to understand for conservation purposeswere observed 1.4 times
more frequently than the next highest response types (physiology and occurrence). Behavioral
metrics, which were studied far more often than other types of responses, may be popular
because they can be simpler to measure and have been proposed as a proxy for demographic
parameters [90]. Nonetheless, behavioral metrics may not reflect the true population consequences of anthropogenic disturbance [91]. Study duration can also influence conclusions;
one long-term study found that low-level recreation had an effect on dolphin habitat use that
was not observed in a short-term behavioral study [81,92], while another found that shortterm behavioral responses did not result in changes in the distribution or relative abundance
of waterbirds [93].
Though most articles documented recreation effects, few presented specific, practical steps
to minimize impacts. About 40% of the articles did not describe any management or mitigation actions, and many more contained only vague suggestions. We see a strong need for
empirical tests of the effectiveness of management actions, which were rare. Encouraging
examples of successful mitigation actions do exist, such as educating divers about avoiding
damage to coral reefs [94], using volunteers to deter harassment of fur seals [95], and installing
fences to establish disturbance-free areas [96,97]. This type of practical evaluation of management strategies is critical in assessing the ability of protected areas to meet demands for both
recreational opportunities and the conservation of biodiversity. Interviewing practitioners
would be a useful direction for future research in order to assess the type and extent of management strategies currently being employed. Even where management recommendations are
provided in the scientific literature, it is unclear to what extent they are received by protected
area managers [98]; a search of unpublished reports and other communications on the subject
would help inform how well conservation scientists are reaching decision-makers.
The effects of recreation on animals is still a relatively unknown and low-profile topic in the
conservation science literature, despite growing evidence that detrimental impacts can occur
from a wide variety of recreational activities. Further, biophysical disturbances associated with
recreation and tourismincluding habitat conversion for roads and resorts, pollution from
vehicles, and the spread of invasive speciesare likely to have additional effects [19], increasing
16 / 21
the overall impact of the recreation and tourism industry. Recreation effects may also act synergistically with other threats to biodiversity such as urbanization and land-use change [18],
which may result in increased access for recreation. This is a troubling problem for managers
and conservation practitioners, since recreation is an integral part of protected areas worldwide [12]. Finding an appropriate balance between biodiversity conservation and outdoor
recreation is complicated, especially since impacts vary among species and recreation activities. We must start by simply acknowledging that these uses are not necessarily compatible for
all species, in all locations. This will make it easier to justify additional research on this topic,
establish restrictions on recreation, and encourage changes in the behavior of recreationists,
leading to improved conservation outcomes.
Supporting Information
S1 Appendix. Articles about recreation effects on animals included in the literature review.
(DOCX)
S1 File. Access database containing information extracted from reviewed papers.
(ACCDB)
S1 Table. PRISMA checklist.
(DOC)
Acknowledgments
We thank A. Hess and P. Turk of the Colorado State University StatLab for helpful statistical
advice. Comments from R. Knight, C. Carroll, and S. Bombaci improved the manuscript.
Author Contributions
Conceptualization: CLL SER AMM KRC.
Data curation: CLL.
Formal analysis: CLL.
Funding acquisition: SER KRC.
Investigation: CLL.
Methodology: CLL SER AMM KRC.
Project administration: SER KRC.
Supervision: SER KRC.
Visualization: CLL.
Writing original draft: CLL.
Writing review & editing: CLL SER AMM KRC.
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Recreation Effects On Wildlife Research

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Recreation Effects On Wildlife Research

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RESEARCH ARTICLE

Effects of Recreation on Animals Revealed as

Outdoor recreation is typically assumed to be compatible with biodiversity conservation and

Competing Interests: Adina Merenlender is on the

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

Screening and data extraction

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

Description or list of categories

Study design Measure of

Was it an experimental study?

Did the study include a control treatment? (e.g. a no-recreation site)

Did the authors find a significant recreation impact?

Positive, negative, unclear

Were multiple species studied?

Amphibian, bird, fish, invertebrate, mammal, reptile

Abundance, behavioral, community (species richness, diversity, or composition), occurrence,

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

Publication trends and geographic distribution

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

Limit recreational access during the breeding season

Restrict boat speed in sensitive areas; prohibit wildlife feeding

Restore habitat; install fencing around sensitive areas

Species translocations; increased use of private land for conservation

Enforce leash laws; keep people on trails

Train staff to recognize signs of animal disturbance

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

Fig 2. Published articles on the effects of non-consumptive recreation on animals by publication

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

Balmford A, Beresford J, Green J, Naidoo R, Walpole M, Manica A. A Global Perspective on Trends in

Losos E, Hayes J, Phillips A, Wilcove D, Alkire C. Taxpayer-Subsidized Resource Extraction Harms

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016

Systematic Review of Recreation Effects on Animals

Kangas K, Luoto M, Ihantola A, Tomppo E, Siikamaki P. Recreation-induced changes in boreal bird

Duffus DA, Dearden P. Non-consumptive wildlife-oriented recreation: A conceptual framework. Biol

PLOS ONE | DOI:10.1371/journal.pone.0167259 December 8, 2016